First record in Mexico of Ceromasia auricaudata Townsend (Diptera: Tachinidae) parasitizing omosus Smith (: Diprionidae)

Álvaro Castañeda-Vildózola1,*, Jesús R. Sánchez-Pale1, Omar Franco-Mora1, and Dulce A. Hernández-Zetina2

The family Diprionidae (Insecta: Hymenoptera), commonly known as of 9-yr-old trees: 17 Pinus gregii Engelm. ex Parl. trees and 14 , includes at least 90 described species and is a group of - Pinus patula Schiede ex Schltdl. & Cham. (Pinaceae). In Oct of the same defoliating in the Northern Hemisphere (Smith 1988; Taeger et yr, 1,500 late stage N. omosus larvae were collected and transported to al. 2010; Smith et al. 2012). Many reports have indicated the presence of the laboratory for conditioning. sawflies of the genusNeodiprion Rohwer, Zadiprion Rohwer, and Monoc- The larvae were placed in 32.5 × 18.0 × 11.5 cm plastic containers tenus Dahlbom (Hymenoptera: Diprionidae) in Mexican conifer forests (Rubbermaid®, Atlanta, Georgia, USA) and fed with pine needles from (Smith 1988; Smith et al. 2010, 2012). Defoliation attributed to sawflies P. gregii that were replaced every 5 d. A total of 1,294 puparia were ob- leads to reduced growth in terms of diam, height, and root size in af- tained and transferred to a new container with previously disinfected fected trees; if attack is severe and prolonged, it can result in tree death, soil with hot water (70 °C for 15 min) as a pupation substrate. The especially among young trees in the sprouting phase (González-Gaona & soil was moistened with distilled water once per wk to avoid desicca- Sánchez-Martínez 2018; Aguilera-Molina et al. 2019). tion and premature death of the pupae. The pupation containers were The genus Neodiprion currently contains 51 described species (Tae- covered with cheesecloth so that parasitoids and adults could ger et al. 2010) of which Neodiprion autumnalis Smith, Neodiprion bi- not escape, and were kept in uncontrolled laboratory conditions. Of color Smith, Neodiprion equalis Smith, and Neodiprion omosus Smith the 1,294 puparia, 1,047 adult sawflies and 11 Tachinidae specimens (all Hymenoptera: Diprionidae) are reported to occur in Mexico (Smith emerged, with a single fly emerging from each puparia. It was identi- 1988). Neodiprion omosus is a univoltine species that is well known fied as C. auricaudata by D. H. Zetina. The specimens were deposited in central Mexico and is associated with 9 species of Pinus L. (Pina- in the Colección de Insectos del Colegio de Postgraduados, Montecillo, ceae) (Cibrián-Tovar et al. 1995; Coria-Avalos et al. 2014). The larvae Texcoco, Estado de Mexico, Mexico. of N. omosus are gregarious, feeding on young needles and the bark of The genus Ceromasia Rondani (Diptera: Tachinidae: Goniini) is young twigs. As they near pupation,N. omosus larvae leave the trees to composed of 3 species: C. auricaudata, Ceromasia hybreas (Walker), overwinter underground as pupae. Adults emerge in summer (Cibrián- and Ceromasia rubrifrons (Macquart) (Diptera: Tachinidae), which are Tovar et al. 1995). recorded from North America, Europe, and Asia (O’Hara et al. 2019). Parasitism is a natural cause of mortality of sawfly larvae (González- The current distribution of C. auricaudata includes Canada and the US Gaona & Sánchez-Martínez 2018). The main groups of parasitoids as- (O’Hara et al. 2019). Our findings contribute to knowledge of range ex- sociated with sawflies include members of the families Ichneumonidae pansion of this species toward central Mexico. Ceromasia auricaudata (Hymenoptera) and Tachinidae (Diptera); however, many reports indi- is a solitary koinobiont endoparasitoid associated with larvae of the cate that ichneumonids account for the majority of cases of parasitism genus Choristoneura Lederer (Lepidoptera: Tortricidae) (O’Hara 2005). in sawfly populations (Ruiz-Cancino & Khalaim 2015; Tao et al. 2016; The literature does not report parasitism of sawflies by members of the Khalaim et al. 2019). Despite the abundance of ichneumonids, the lit- genus Ceromasia; as such, our findings are also a new host-parasitoid erature cites 31 genera of Tachinidae associated with sawflies (Rich- interaction for Mexico, increasing the number of genera of Tachini- ter & Kasparyan 2013). In this study, we report for the first time the dae associated with sawflies previously cited by Richter & Kasparyan presence of Ceromasia auricaudata Townsend (Diptera: Tachinidae) in (2013). Other cases of parasitism of sawfly larvae attributed to Tachini- Mexico in association with larvae of the sawfly N. omosus, which con- dae in Mexico include Spathimeigenia (Vibrissina) mexicana (Aldrich) stitutes a new host record. (Diptera: Tachinidae) parasitizing larvae of Zadiprion falsus Smith (Hy- In Aug 2018, we observed an outbreak of N. omosus larvae in the menoptera: Diprionidae) in Michoacán (Méndez 1983); Lespesia pos- experimental station of the Facultad de Ciencias Agrícolas de la Uni- tica (Walker) and V. mexicana (Diptera: Tachinidae) parasitizing larvae versidad Autónoma del Estado de México, located in the community of sanchezi Smith (Hymenoptera: Diprionidae) in San of the Cerrillo, Piedras Blancas (19.2432°N, 99.4120°W; 2,614 masl), Luis Potosí (Ordaz-Silva et al. 2014); and Chetogena (Diplostichus) nr. Toluca, Estado de Mexico, Mexico. The outbreak affected 2 populations lophyri (Townsend) (Diptera: Tachinidae) reported as a parasitoid of

1Facultad de Ciencias Agrícolas, Universidad Autónoma del Estado de Mexico, Campus El Cerrillo, Toluca, Estado de Mexico, C.P. 50200, Mexico; E-mail: [email protected] (A. C.-V.), [email protected] (J. R. S.-P.), [email protected] (O. F.-M.) 2Instituto Interamericano de Cooperación para la Agricultura (IICA), Servicio Nacional de Sanidad, Inocuidad y Calidad Agroalimentaria, Unidad Integral de Diagnóstico, Servicio y Constatación, Carretera Federal Mexico- Pachuca Km. 37.7, Tecámac, Estado de Mexico, C.P. 55740, Mexico; E-mail: [email protected] (D. A. H.-Z.) *Corresponding author; E-mail: [email protected]

146 2021 — Florida Entomologist — Volume 104, No. 2 Scientific Notes 147 Zadiprion rohweri Middleton (Hymenoptera: Diprionidae) in Coahuila and future impacts of diprionid sawflies on the pine forests of North-West- (Smith et al. 2016). ern Mexico. Peer Journal 7: e7220. doi: 10.7717/peerj.7220 Other parasitoids that emerged from N. omosus in this study in- Cibrián-Tovar J, Méndez-Montiel MT, Campos-Bolaños R, Yates III HO, Flores- Lara JE. 1995. Insectos forestales de México. Universidad Autónoma Chap- cluded the ichneumonids Lamachus cushmani Khaleim & Ruiz-Cancino ingo, Chapingo, México. and Lamachus toluca Khaleim & Ruiz-Cancino (Hymenoptera: Ichneu- Coppel HC, Maw MG. 1954. Studies on dipterous parasites of the spruce bud- monidae), previously described by Khaleim et al. (2019). worm, Choristoneura fumiferana (Clem.) (Lepidoptera: Tortricidae). III. According to O’Hara (2005), C. auricaudata eggs are deposited on- Ceromasia auricaudata Tns. (Diptera: Tachinidae). Canadian Journal of Zo- ology 32: 144–156. to foliage and do not hatch until they are ingested by a potential host. Coria-Avalos VM, González-Gaona E, Pulido-Herrera A, Muñoz-Flores HJ. 2014. This reproductive strategy leads to a low probability of parasitism, but Detección y descripción morfológica de “mosca sierra” en bosques de la co- is much more efficient than other tachinids with more conventional munidad indígena de nuevo San Juan Parangaricutiro, Michoacán, México. strategies. Ceromacia auricaudata overwintered as a larvae within an Entomología Mexicana 1: 426–430. overwintering N. omosus prepupae. In this study, average time from González-Gaona E, Sánchez-Martínez G. 2018. Identificación y manejo de mos- cas sierra de la familia Diprionidae presentes en el centro norte de México. the collection of parasitized larvae to the emergence of adult parasit- Folleto Técnico. Fondo Sectorial para la Investigación, el Desarrollo y la In- oids was 297.72 d (n = 11, 170–340 days). Coppel & Maw (1954) point- novación Tecnológica Forestal (CONACYT-CONAFOR). Pabellón de Arteaga, ed out that adult C. auricaudata required 9 to 11 d to emerge from Aguascalientes, Mexico. their primary host, Choristoneura fumiferana (Clemens) (Lepidoptera: Khalaim AI, Ruiz-Cancino E, Coronado-Blanco JM, Castañeda-Vildózola Á. 2019. First record of the genus Lamachus Förster, 1869 (Hymenoptera: Ctenopel- Tortricidae). Despite the ecological and behavioral similarity between matinae) from Mexico, with description of two new species. Russian Ento- diprionid and lepidopteran larvae, the use of sawfly larvae as potential mological Journal 28: 169–179. hosts by tachinids has not been successful particularly from an evolu- Méndez MT. 1983. Evaluación del ataque de Zadiprion vallicola Rohwer (Hy- tionary perspective, such that parasitism of diprionids by tachinids is menoptera: Diprionidae) defoliador de pinos, sobre el crecimiento e incre- apparently secondary (Richter & Kasparyan 2013). This behavior may mento en diámetro de Pinus montezumae Lamb., en la Meseta Tarasca. Tesis de Licenciatura, Departamento de Parasitología Agrícola. Universidad explain why only 0.85% of N. omosus larvae were naturally parasitized Autónoma Chapingo, Chapingo. México. by C. auricaudata in the study site. O’Hara JE. 2005. A review of the tachinid parasitoids (Diptera: Tachinidae) of Ne- We thank the Universidad Autónoma del Estado de México and arctic Choristoneura species (Lepidoptera: Tortricidae), with keys to adults the Secretaria de Investigación y Estudios Avanzados for financing this and puparia. Zootaxa 938: 1–46. O’Hara JE, Henderson SJ, Wood DM. 2019. Preliminary checklist of the Tach- project as part of grant 4795/2019CIB. Thanks to Lynna M. Kiere for inidae of the world. Version 1.0. http://www.nadsdiptera.org/Tach/World- assistance in revision of our manuscript. Tachs/Checklist/Worldchecklist.html (last accessed 19 Dec 2020). Ordaz-Silva S, Gallegos-Morales G, Sánchez-Peña SR, Flores-Dávila M, Salas- Marina MÁ, Landeros-Flores J. 2014. First records of Lespesia postica and Summary Vibrissina mexicana (Tachinidae) as parasitoids of Monoctenus sanchezi (Di- prionidae). Southwestern Entomologist 39: 511–516. Richter VA, Kasparyan DR. 2013. Tachinid (Diptera, Tachinidae) Parasitoids of Ceromasia auricaudata Townsend (Diptera: Tachinidae) is recorded sawflies (Hymenoptera, Symphyta). Entomological Review 93: 630–633. for the first time in Mexico. This also is the first time thatC. auricaudata is Ruiz-Cancino E, Khalaim AI. 2015. Mexican species of the genus Exenterus Hartig associated with Neodiprion omosus Smith (Hymenoptera: Diprionidae), (Hymenoptera: Ichneumonidae: Tryphoninae) reared from diprionid hosts. increasing the number of genera of Tachinidae associated with sawflies. Zootaxa 4048: 140–150. Smith DR. 1988. 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